Abstract

The visual system is highly variable across species, and such variability is a key factor influencing animal behavior. Variation in the visual system, for instance, can influence the outcome of learning tasks when visual stimuli are used. We illustrate this issue in guppies (Poecilia reticulata) artificially selected for large and small relative brain size with pronounced behavioral differences in learning experiments and mate choice tests. We performed a study of the visual system by quantifying eye size and optomotor response of large-brained and small-brained guppies. This represents the first experimental test of the link between brain size evolution and visual acuity. We found that female guppies have larger eyes than male guppies, both in absolute terms and in relation to their body size. Likewise, individuals selected for larger brains had slightly larger eyes but not better visual acuity than small-brained guppies. However, body size was positively associated with visual acuity. We discuss our findings in relation to previous macroevolutionary studies on the evolution of brain morphology, eye morphology, visual acuity, and ecological variables, while stressing the importance of accounting for sensory abilities in behavioral studies.Significance statementPre-existing perceptual biases can be keys for the development of specific behavioral patterns. Hence, potential differences in sensory systems need to be taken into account in the study of animal behavior. We highlight this necessity concentrating on the visual domain and using experimental data on brain size-selected guppies in which we assessed eye size and visual acuity. Behavioral differences between large-brained and small-brained guppies in learning and mate choice predominantly relied on tests using visual cues. Analyses of visual capabilities in this system are therefore necessary. Furthermore, this system offers the unprecedented opportunity to experimentally test the relationship between brain size, eye morphology, and visual capabilities. Our results show similar visual acuities between large-brained and small-brained guppies. However, the differences observed in eye area between the sexes, together with the observed positive relationship between body size and visual acuity, highlight the need to incorporate perceptive differences in the study of animal behavior.

Highlights

  • Sensory systems provide the interface between organisms and their environment and are crucial for an individual’s fitness

  • Analyses combining all stimuli showed that fish spent a much larger proportion of time circling when presented with a rotational stimulus than when presented with static images of stimuli

  • LMMoptomotor response: sex: χ2 = 8.05, df = 1, p = 0.004; Fig. 5), this difference was likely driven by their larger body size since we found no effect of sex on optomotor response when controlling for body size (LMMoptomotor response: sex: χ2 = 0.01, df = 1, p = 0.974)

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Summary

Introduction

Sensory systems provide the interface between organisms and their environment and are crucial for an individual’s fitness. The visual system is important for a wide range of species, including humans, when foraging, selecting a mate, or escaping from potential predators. In such species, visual abilities should be strongly influenced by natural selection. Visual abilities vary markedly across species in the animal kingdom. Visual acuity, the ability of an individual to discriminate spatial detail (Land and Nilsson 2012), varies dramatically even within the closely related species of poeciliid fishes (Douglas and Hawryshyn 1990). Differences in ecological requirements form one important factor shaping visual evolution across species

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